Phylogeographic, toxicological and ecological evidence for the global distribution of Raphidiopsis raciborskii and its northernmost presence in Lake Nero, Central Western Russia

Abstract

Raphidiopsis raciborskii is a freshwater, potentially toxigenic cyanobacterium, originally described as a tropical species that is spreading to northern regions over several decades. The ability of R. raciborskii to produce cyanotoxins - in particular the alkaloid cylindrospermopsin (CYN), which is toxic to humans and animals - is of serious concern. The first appearance of R. raciborskii in Russia was noted in Lake Nero in the summer of 2010. This is the northernmost (57°N) recorded case of the simultaneous presence of R. raciborskii and detection of CYN. In this study, the data from long-term monitoring of the R. raciborskii population, temperature and light conditions in Lake Nero were explored. CYN and cyr/aoa genes present in environmental samples were examined using HPLC/MS-MS and PCR analysis. A R. raciborskii strain (R104) was isolated and its morphology, toxigenicity and phylogeography were studied. It is supposed that the trigger factor for the strong development of R. raciborskii in Lake Nero in summer 2010 may have been the relatively high water temperature, reaching 29-30 °C. Strain R. raciborskii R104 has straight trichomes and can produce akinetes, making it morphologically similar to European strains. Phylogeographic analysis based on nifH gene and 16S-23S rRNA ITS1 sequences showed that the Russian strain R104 grouped together with R. raciborskii strains isolated from Portugal, France, Germany and Hungary. The Russian strain R104 does not contain cyrA and cyrB genes, meaning that it - like all European strains - cannot produce CYN. Thus, while recent invasion of R. raciborskii into Lake Nero has occurred, morphological, genetic, and toxicological data supported the spreading of this cyanobacterium from other European lakes. Detection of CYN and cyr/aoa genes in environmental samples indicated the cyanobacterium Aphanizomenon gracile as a likely producer of CYN in Lake Nero. The article also discusses data on the global biogeography of R. raciborskii. Genetic similarity between R. raciborskii strains isolated from very remote continents might be related to the ancient origin of the cyanobacterium inhabiting the united continents of Laurasia and Gondwana, rather than comparably recent transoceanic exchange between R. raciborskii populations.

Keywords: Aphanizomenon gracile; Lake Nero; Phylogeography; Raphidiopsis raciborskii; Water temperature; Сylindrospermopsin.